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Profiling the Secretome of Human Stem Cells from Dental Apical Papilla

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Profiling the Secretome of Human Stem Cells from Dental Apical Papilla STEM CELLS AND DEVELOPMENT Volume 25, Number 6, 2016 Ó Mary Ann Liebert, Inc. DOI: 10.1089/scd.2015.0298 Profiling the Secretome of Human Stem Cells from Dental Apical Papilla Shi Yu,1 Yuming Zhao,1 Yushi Ma,2 and Lihong Ge1 Recent studies have shown that secretion of bioactive factors from mesenchymal stem cells (MSCs) plays a primary role in MSC-mediated therapy; especially for bone marrow-derived MSCs (BMSCs). MSCs from dental apical papilla (SCAPs) are involved in root development and may play a critical role in the formation of dentin and pulp. Bioactive factors secreted from SCAPs actively contribute to their environment; however, the SCAPs secretome remains unclear. To address this and gain a deeper understanding of the relevance of SCAPs secretions in a clinical setting, we used isobaric chemical tags and high-performance liquid chromatography with tandem mass spectrometry to profile the secretome of human SCAPs and then compared it to that of BMSCs. A total of 2,046 proteins were detected from the conditioned medium of SCAPs, with a false discovery rate of less than 1.0%. Included were chemokines along with angiogenic, immunomodulatory, antiapoptotic, and neuroprotective factors and extracellular matrix (ECM) proteins. The secreted levels of 151 proteins were found to differ by at least twofold when BMSCs and SCAPs were compared. Relative to BMSCs, SCAPs exhibited increased secretion of proteins that are involved in metabolic processes and transcription and lower levels of those associated with biological adhesion, developmental processes, and immune function. In addition, SCAPs secreted significantly larger amounts of chemokines and neurotrophins than BMSCs, whereas BMSCs secreted more ECM proteins and proangiogenic factors. These results may provide important clues regarding the molecular mechanisms associated with tissue regeneration and how they differ between cell sources. Introduction ment [10], and in combination with tissue engineering pro- cedures, Huang et al. used SCAPs to regenerate vascularized he secretions of mesenchymal stem cells (MSCs) human dental pulp in an emptied root canal and this was Thave gained considerable attention in recent years, par- accompanied by formation of new dentin on the existing ticularly with regard to MSC-mediated therapy and tissue dentinal wall [11]. However, the understanding of SCAPs regeneration. This has resulted in a large body of evidence function and relevance in a clinical setting needs to be im- suggesting that differentiation of MSCs into multiple cell proved. One means to achieve this is identification of the types is limited under in vivo conditions and the secretion of wide array of proteins they secrete. bioactive factors from the MSCs themselves plays a critical Therefore, in this study, we investigated the secretome of role [1–3]. MSCs actively contribute to their environment by human SCAPs and compared the resulting profile to that of releasing trophic (antiapoptotic, supportive, angiogenic, etc.) BMSCs, with the aim of achieving insights into the func- factors, immunomodulatory factors, and chemoattractants tional role of SCAPs secretions and the molecular basis of that act either on themselves or on neighboring cells [4]. their actions. Various studies have shown that the use of bone marrow- derived MSC (BMSC)-derived conditioned media (CM) alone without cell transplantation can induce tissue repair, Materials and Methods including that of bone and nerves [5–7]. Establishment, characterization, and analysis Stem cells from dental apical papilla (SCAPs) are found of cell proliferation rate of SCAPs in the root apex of immature permanent teeth [8]. These and BMSCs cultures cells appear to be the source of odontoblasts and contribute to root formation [9]. For example, interruption of SCAPs Normal human impacted third molars with immature roots development was found to result in a halted root develop- were collected from healthy patients (aged 16–24 years) 1Department of Pediatric Dentistry, Peking University School and Hospital of Stomatology, Peking University Health Science Center, Peking University, Beijing, China. 2The Department of Orthodontics Center for Craniofacial Stem Cell Research and Regeneration, Beijing, China. 499 500 YU ET AL. (n = 5). Bone marrows were obtained from the mandibular (release 2014_04_10; 20,264 reviewed entries) was used to bone of healthy patients (aged 20–30 years) (n = 3). Sample search. A fragment-ion mass tolerance of 0.050 Da and a collection was approved by the Ethics Committee of the parent-ion tolerance of 10.0 ppm were equipped for Mascot. Health Science Center of Peking University (Beijing, China; Scaffold Q+ version 4.4.1.1 (Proteome Software, Inc.) IRB00001052-11060). SCAPs and BMSCs were isolated was used to assess label-based peptide quantification and from dental apical papilla tissues and mandibular bone mar- protein identification. Peptide identifications were accepted row, respectively. Cultures of MSCs were maintained in if the false discovery rate (FDR) was less than 1.0%, and alpha-modified Eagle’s minimum essential medium (Gibco) protein identifications were accepted if the probability was supplemented with 10% fetal bovine serum (Gibco) in 5% more than 66.0% and at least one identified peptide was carbon dioxide at 37°C. The cells were used in experiments contained. Acquired intensities in the experiment were after three to five passages, and for each experiment, SCAPs globally normalized across all acquisition runs. Individual and BMSCs had the same passage number. quantitative samples were normalized within each acquisi- SCAPs and BMSCs were characterized by flow cytometry tion run. The intensity of each peptide identified was nor- using fluorescein-isothiocyanate-conjugated or phycoerythrin- malized within the assigned protein. The reference channels conjugated antibodies specific for CD73, CD90, CD105, were normalized to produce a 1:1 ratio. All normalization CD146, and CD34 (BD Biosciences) as previously described. calculations were performed using medians to multiplica- MSCs were seeded into 96-well plates at a density of 1.0 · tively normalize the data. Differentially expressed proteins 103 cells/well and then cultured for 7 days. Cell counting kit were determined using a Kruskal–Wallis test. String soft- 8 (CCK-8; Dojindo) solution was added to each well of the ware (http://string-db.org/) was employed to visualize pro- plate and the absorbance was measured at 450 nm, every 24 h, tein interaction networks between the secretory proteins of according to the manufacturer’s protocol. SCAPs. Functional annotation analysis using gene ontology (GO) terms was performed using the DAVID Bioinfor- Preparation of CM and protein digestion matics Resources 6.7 (http://david.abcc.ncifcrf.gov/) and PANTHER (protein analysis through evolutionary relation- SCAPs and BMSCs were seeded on 100-mm plates at a ships) classification system (www.pantherdb.org/). density of 20,000 cells/cm2. When MSCs reached 90% confluency, they were washed five times with phosphate- buffered saline and cultured in serum-free medium for 24 h. Western blotting The CM were collected after centrifugation at 130 g for Thirty micrograms of secretory protein were separated 10 min to remove the cellular debris and then passed through by 10% sodium dodecyl sulfate–polyacrylamide gel elec- a 0.22-mm filter. The samples were concentrated, then air- trophoresis and transferred on a polyvinylidene fluoride dried, redissolved in triethylammonium bicarbonate (Pro- membrane. The membrane was blocked with 5% (w/v) nonfat mega), and finally, reduced with dithiothreitol at 55°C for dried milk, incubated overnight at 4°C with primary antibodies 1 h. Next, iodoacetamide (Promega) was added to the sam- against midkine (MDK) and angiopoietin-related protein 2 ples and they were left for 1 h at room temperature, pro- (ANGPTL2; Abcam), and then reacted with horseradish- tected from light. Protein concentration was determined peroxidase-conjugated secondary antibodies (Origene). using a bicinchoninic acid (Thermo Fisher Scientific) assay. Immunoreactive bands were visualized by enhanced chemi- luminescence (Cwbiotech) at room temperature and then TMT and HPLC-MS/MS analysis digitized using the Fusion FX image analyzer (Viber Loumat). Samples were digested with sequence-grade modified trypsin (Promega) and then labeled using the TMT reagent kit Real-time reverse transcription-polymerase (Thermo Fisher Scientific) [12]. Ten fractions were collected chain reaction analysis by high-pH separation using an Aquity UPLC system (Waters Corporation) [13]. Total RNA was extracted from SCAPs and BMSCs (after The fractions were resuspended in formic acid, separated the culture procedure described above) using TRIzol Reagent by nanoLC, and analyzed by online electrospray tandem mass (Invitrogen) according to the manufacturer’s instructions. spectrometry. The analysis was performed with nanoAquity cDNA was synthesized with oligo(dT) primers using a re- UPLC system (Waters Corporation), which was equipped verse transcriptase kit (Promega). The primer sequences were with an online nanoelectrospray ion source and connected to designed by primer bank (Supplementary Table S1; Supple- a Q-Exactive hybrid quadrupole-orbitrap mass spectrometer mentary Data are available online at www.liebertpub.com/ (Thermo Fisher Scientific). Samples were separated by ana- scd). Quantitative reverse transcription polymerase chain re- lytical column (Thermo Scientific Acclaim PepMap C18, action (qRT-PCR) was carried out
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